diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 8c8f342e1..573d9a910 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -292,10 +292,7 @@ func NewLocalBackend(logf logger.Logf, logID logid.PublicID, sys *tsd.System, lo
 	osshare.SetFileSharingEnabled(false, logf)
 
 	ctx, cancel := context.WithCancel(context.Background())
-	portpoll, err := portlist.NewPoller()
-	if err != nil {
-		logf("skipping portlist: %s", err)
-	}
+	portpoll := new(portlist.Poller)
 
 	b := &LocalBackend{
 		ctx:            ctx,
@@ -1377,7 +1374,6 @@ func (b *LocalBackend) Start(opts ipn.Options) error {
 
 	if b.portpoll != nil {
 		b.portpollOnce.Do(func() {
-			go b.portpoll.Run(b.ctx)
 			go b.readPoller()
 
 			// Give the poller a second to get results to
@@ -1812,11 +1808,30 @@ func dnsMapsEqual(new, old *netmap.NetworkMap) bool {
 // readPoller is a goroutine that receives service lists from
 // b.portpoll and propagates them into the controlclient's HostInfo.
 func (b *LocalBackend) readPoller() {
-	n := 0
+	isFirst := true
+	ticker := time.NewTicker(portlist.PollInterval())
+	defer ticker.Stop()
+	initChan := make(chan struct{})
+	close(initChan)
 	for {
-		ports, ok := <-b.portpoll.Updates()
-		if !ok {
+		select {
+		case <-ticker.C:
+		case <-b.ctx.Done():
 			return
+		case <-initChan:
+			// Preserving old behavior: readPoller should
+			// immediately poll the first time, then wait
+			// for a tick after.
+			initChan = nil
+		}
+
+		ports, changed, err := b.portpoll.Poll()
+		if err != nil {
+			b.logf("error polling for open ports: %v", err)
+			return
+		}
+		if !changed {
+			continue
 		}
 		sl := []tailcfg.Service{}
 		for _, p := range ports {
@@ -1840,8 +1855,8 @@ func (b *LocalBackend) readPoller() {
 
 		b.doSetHostinfoFilterServices(hi)
 
-		n++
-		if n == 1 {
+		if isFirst {
+			isFirst = false
 			close(b.gotPortPollRes)
 		}
 	}
diff --git a/portlist/poller.go b/portlist/poller.go
index 16dd8e74c..90c8e7838 100644
--- a/portlist/poller.go
+++ b/portlist/poller.go
@@ -9,6 +9,7 @@
 import (
 	"context"
 	"errors"
+	"fmt"
 	"runtime"
 	"sync"
 	"time"
@@ -17,9 +18,16 @@
 	"tailscale.com/envknob"
 )
 
-var pollInterval = 5 * time.Second // default; changed by some OS-specific init funcs
+var (
+	pollInterval         = 5 * time.Second // default; changed by some OS-specific init funcs
+	debugDisablePortlist = envknob.RegisterBool("TS_DEBUG_DISABLE_PORTLIST")
+)
 
-var debugDisablePortlist = envknob.RegisterBool("TS_DEBUG_DISABLE_PORTLIST")
+// PollInterval is the recommended OS-specific interval
+// to wait between *Poller.Poll method calls.
+func PollInterval() time.Duration {
+	return pollInterval
+}
 
 // Poller scans the systems for listening ports periodically and sends
 // the results to C.
@@ -37,8 +45,9 @@ type Poller struct {
 	// addProcesses is not used.
 	// A nil values means we don't have code for getting the list on the current
 	// operating system.
-	os     osImpl
-	osOnce sync.Once // guards init of os
+	os       osImpl
+	initOnce sync.Once // guards init of os
+	initErr  error
 
 	// closeCtx is the context that's canceled on Close.
 	closeCtx       context.Context
@@ -69,24 +78,23 @@ type osImpl interface {
 // newOSImpl, if non-nil, constructs a new osImpl.
 var newOSImpl func(includeLocalhost bool) osImpl
 
-var errUnimplemented = errors.New("portlist poller not implemented on " + runtime.GOOS)
+var (
+	errUnimplemented = errors.New("portlist poller not implemented on " + runtime.GOOS)
+	errDisabled      = errors.New("portlist disabled by envknob")
+)
 
 // NewPoller returns a new portlist Poller. It returns an error
 // if the portlist couldn't be obtained.
 func NewPoller() (*Poller, error) {
-	if debugDisablePortlist() {
-		return nil, errors.New("portlist disabled by envknob")
-	}
 	p := &Poller{
 		c:       make(chan List),
 		runDone: make(chan struct{}),
 	}
-	p.closeCtx, p.closeCtxCancel = context.WithCancel(context.Background())
-	p.osOnce.Do(p.initOSField)
-	if p.os == nil {
-		return nil, errUnimplemented
+	p.initOnce.Do(p.init)
+	if p.initErr != nil {
+		return nil, p.initErr
 	}
-
+	p.closeCtx, p.closeCtxCancel = context.WithCancel(context.Background())
 	// Do one initial poll synchronously so we can return an error
 	// early.
 	if pl, err := p.getList(); err != nil {
@@ -103,10 +111,18 @@ func (p *Poller) setPrev(pl List) {
 	p.prev = slices.Clone(pl)
 }
 
-func (p *Poller) initOSField() {
-	if newOSImpl != nil {
-		p.os = newOSImpl(p.IncludeLocalhost)
+// init initializes the Poller by ensuring it has an underlying
+// OS implementation and is not turned off by envknob.
+func (p *Poller) init() {
+	if debugDisablePortlist() {
+		p.initErr = errDisabled
+		return
 	}
+	if newOSImpl == nil {
+		p.initErr = errUnimplemented
+		return
+	}
+	p.os = newOSImpl(p.IncludeLocalhost)
 }
 
 // Updates return the channel that receives port list updates.
@@ -115,14 +131,18 @@ func (p *Poller) initOSField() {
 func (p *Poller) Updates() <-chan List { return p.c }
 
 // Close closes the Poller.
-// Run will return with a nil error.
 func (p *Poller) Close() error {
-	p.closeCtxCancel()
-	<-p.runDone
-	if p.os != nil {
-		p.os.Close()
+	if p.initErr != nil {
+		return p.initErr
 	}
-	return nil
+	if p.os == nil {
+		return nil
+	}
+	if p.closeCtxCancel != nil {
+		p.closeCtxCancel()
+		<-p.runDone
+	}
+	return p.os.Close()
 }
 
 // send sends pl to p.c and returns whether it was successfully sent.
@@ -137,6 +157,24 @@ func (p *Poller) send(ctx context.Context, pl List) (sent bool, err error) {
 	}
 }
 
+// Poll returns the list of listening ports, if changed from
+// a previous call as indicated by the changed result.
+func (p *Poller) Poll() (ports []Port, changed bool, err error) {
+	p.initOnce.Do(p.init)
+	if p.initErr != nil {
+		return nil, false, fmt.Errorf("error initializing poller: %w", p.initErr)
+	}
+	pl, err := p.getList()
+	if err != nil {
+		return nil, false, err
+	}
+	if pl.equal(p.prev) {
+		return nil, false, nil
+	}
+	p.setPrev(pl)
+	return p.prev, true, nil
+}
+
 // Run runs the Poller periodically until either the context
 // is done, or the Close is called.
 //
@@ -179,10 +217,13 @@ func (p *Poller) runWithTickChan(ctx context.Context, tickChan <-chan time.Time)
 }
 
 func (p *Poller) getList() (List, error) {
-	if debugDisablePortlist() {
+	// TODO(marwan): this method does not
+	// need to do any init logic. Update tests
+	// once async API is removed.
+	p.initOnce.Do(p.init)
+	if p.initErr == errDisabled {
 		return nil, nil
 	}
-	p.osOnce.Do(p.initOSField)
 	var err error
 	p.scratch, err = p.os.AppendListeningPorts(p.scratch[:0])
 	return p.scratch, err
diff --git a/portlist/portlist_test.go b/portlist/portlist_test.go
index 6055a8426..86e8bd335 100644
--- a/portlist/portlist_test.go
+++ b/portlist/portlist_test.go
@@ -175,12 +175,33 @@ func TestEqualLessThan(t *testing.T) {
 	}
 }
 
+func TestClose(t *testing.T) {
+	var p Poller
+	err := p.Close()
+	if err != nil {
+		t.Fatal(err)
+	}
+	p = Poller{}
+	_, _, err = p.Poll()
+	if err != nil {
+		t.Skipf("skipping due to poll error: %v", err)
+	}
+	err = p.Close()
+	if err != nil {
+		t.Fatal(err)
+	}
+}
+
 func TestPoller(t *testing.T) {
 	p, err := NewPoller()
 	if err != nil {
 		t.Skipf("not running test: %v", err)
 	}
-	defer p.Close()
+	t.Cleanup(func() {
+		if err := p.Close(); err != nil {
+			t.Errorf("error closing poller in test: %v", err)
+		}
+	})
 
 	var wg sync.WaitGroup
 	wg.Add(2)